Inhibition of the bioavailability of heavy metals in sewage ... - PLOS

RESEARCH ARTICLE

Inhibition of the bioavailability of heavy metals in sewage sludge biochar by adding two stabilizers Zhujian Huang1,2, Qin Lu1, Jun Wang1, Xian Chen1, Xiaoyun Mao1*, Zhenli He3

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OPEN ACCESS Citation: Huang Z, Lu Q, Wang J, Chen X, Mao X, He Z (2017) Inhibition of the bioavailability of heavy metals in sewage sludge biochar by adding two stabilizers. PLoS ONE 12(8): e0183617. https://doi. org/10.1371/journal.pone.0183617 Editor: Jorge Paz-Ferreiro, RMIT University, AUSTRALIA Received: April 6, 2017 Accepted: August 8, 2017 Published: August 23, 2017 Copyright: © 2017 Huang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: This work was supported by the grants (51509093) from Natural Science Foundation of China, the grants (2016B020242005, 2015B020215012, 2014A050503065 and 2017A020216025) from the Science and Technology Project of Guangdong Province, the grants (201508030039 and 201504282153571) from the Science and Technology Project of Guangzhou City and the grant (2016K0014) from

1 College of Natural Resources and Environment, South China Agricultural University, Guangzhou, China, 2 Guangdong Provincial Key Laboratory of Environmental Pollution Control and Remediation Technology, Guangzhou, P. R. China, 3 Indian River Research and Education Center, Institute of Food and Agricultural Sciences, University of Florida, Fort Pierce, FL, United States of America * [email protected]

Abstract Agricultural application of sewage sludge (SS) after carbonization is a plausible way for disposal. Despite its benefits of improving soil fertility and C sequestration, heavy metals contained in sewage sludge biochars (SSB) are still a concern. In this study, two types of heavy metal stabilizers were chosen: fulvic acid (FA) and phosphogypsum (with CaSO4, CS, as the main component). The two stabilizers were incorporated into SS prior to 350˚C carbonization for 1 h at the rates of 1%, 2%, or 4%. The obtained SSBs were then analyzed by Fourier transform infrared spectroscopy (FTIR) and X-ray photoelectron spectroscopy (XPS). Total and available concentrations of four heavy metals, i.e., Zn, Pb, Cd, and Ni, in the SSBs were determined. In addition, a series of pot soil culture experiments was conducted to investigate the effects of stabilizers incorporation into SSB on heavy metal bioavailability and the uptake by plants (corn as an indicator) and plant biomass yield, with SS and SSB (no stabilizers) as controls. The results showed that incorporation of both FA and CS increased functional groups such as carboxyl, phenol, hydroxyl, amine and quinine groups in the SSBs. The percentage of heavy metals in sulfuric and oxidizable state and residual state of SSBs were significantly increased after carbonization, and hence the mobility of the heavy metals in SSBs was decreased. The introduction of the stabilizers (i.e., FA or CS) significantly lowered the total and available concentrations of Zn, Pb, Cd, and Ni. The reduction in available heavy metal concentration increased with incorporation rate of the stabilizers from 1% to 4%. In the treatments with FA or CS incorporated SSB, less heavy metals were taken up by plants and more plant biomass yields were obtained. The mitigating effects were more pronounced at higher rates of FA or CS stabilizer. These findings provide a way to lower bioavailability of heavy metals in SS or SSB for land application or horticulture as a peat substitute.

PLOS ONE | https://doi.org/10.1371/journal.pone.0183617 August 23, 2017

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Inhibition of heavy metals in sewage sludge biochar

the Research Fund Program of Guangdong Provincial Key Laboratory of Environmental Pollution Control and Remediation Technology. Competing interests: The authors have declared that no competing interests exist.

Introduction With increasing population and urbanization, huge amounts of sewage sludge (SS) are produced every day. In China, approximately 12.53 million tons of SS is produced each year [1]. Disposal and/or beneficial utilization of the ever increasing SS have become a challenge worldwide. Recently, SS carbonization has been considered as an environmentally friendly way of SS treatment. The resulting product, SS biochar (SSB), can be used as soil amendment to increase soil organic matter, improve soil fertility, and remediate polluted soils by heavy metals or organic contaminants [2,3]. Recently, it was found that SSB can been explored on as a peat substitute for growing media components, which can increase the N, P and K content of growing media [3]. However, SS itself contains heavy metals and therefore, SSB usually contains more heavy metals than biochars made from plant residues [4]. As metals are non-biodegradable; they may be released from SSB, taken up by plants, and amplify along the food chains, and eventually pose a threat to ecosystem functions and/or human health. Therefore, the heavy metals in SSB need to be stabilized to minimize their environmental risk. Common metal stabilizers include zeolite [5], red mud, apatite [6], sepiolite [7], fly ash [8], iron/manganese oxides [1], phosphates, limestone and Ca-rich materials [9]. The mechanisms of stabilization include surface adsorption, precipitation, formation of stable complexes, and ligands or ion exchange [10]. For example, phosphate rock immobilizes Pb from aqueous solutions and soils through the formation of solid pyromorphite-like minerals [11]. Studies have shown positive effects of stabilizer application on lowering heavy metal availability in contaminated soils. But little research has been conducted to investigate the effects of stabilizers on heavy metal availability in SSB. In this study, two types of stabilizers (fulvic acid, FA, and calcium sulfate, CS), incorporated at different rates, were investigated for their effects on the available concentrations of four heavy metals (i.e., Zn, Pb, Cd, and Ni) in SSB. In addition, a soil pot experiment was conducted to investigate effect of SSB with stabilizer incorporation on heavy metal uptake by plants and plant biomass yield.

Materials and methods Materials and apparatus The sewage sludge (SS) is secondary sludge (excess activated sludge out of system) obtained aerobic treatment of sludge from the secondary sedimentation tank of the activated sludge system in Guangzhou Liede domestic sewage treatment plant (using improved A2/O process) in Guangzhou, Guangdong Province, China. We have got the permission from the managers of domestic sewage treatment plant. After transported to the laboratory, the SS was air-dried for 2 d, oven-dried at 60 oC to constant weight, ground and passed through a 40-mesh sieve prior to use. The organic stabilizer used in this study was weathered coal. Since FA is the main component of the weathered coal [12], hereafter. FA is used to stand for this stabilizer. The inorganic stabilizer was phosphogypsum with CaSO4 (CS) as the main component. Hereafter, CS is used to stand for this stabilizer. Phosphogypsum (also named ardealite) is a by-product of the phosphate fertilizer industry. It is formed by the chemical attack of the phosphate rock withesulphuric acid to produce phosphoric acid. This waste is generally stored in piles near the fertilizer factory, whose main ingredient is gypsum (chemical component is CaSO4) [13]. The radioactive activity (176 Bqkg-1) of the phosphogypsum we used is safe for using as building materials in China (GB 6566–2010). The quantity of the phosphogypsum added to the soil is very low, and also safe in the application of soil amendment. The soil used in the pot experiment was collected from the campus of South China Agricultural University. It is uduits, with a pH of 6.2, a CEC of 8.35 C molKg-1, an EC of 156 uS/cm (s/w = 1:5), an organic matter


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Table 1. Heavy metal concentrations (mg/kg) of the soil, sewage sludge (SS), fulvic acid (FA) and phosphogypsum (CS). Zn

Pb

Cd

Ni

Total

Available

Total

Available

Total

Available

Total

Available

Soil

70.11

7.24

32.78

1.30

0.45

0.09

16.90

0.26

SS

764.20

354.54

119.70

28.71

3.00

1.42

49.90

22.65

FA

29.72

10.23

11.88

2.55

0.21

0.03

4.64

0.92

CS

31.21

13.72

29.07

3.36

0.28

0.06

1.39

0.05

https://doi.org/10.1371/journal.pone.0183617.t001

content of 0.5%,and available N, P, and K of 33 mg N/kg, 6 mg P/kg, and 50 mg K/kg, respectively. The organic matter content and EC of SS were 53.02% and 1030 uS/cm (s/w = 1:5), respectively. The heavy metal concentrations of the soil, SS and FA are shown in Table 1. Fourier transform infrared (FTIR) spectra were recorded between 4000 cm-1 and 400 cm-1 using a Hitachi EPI-G2 infrared spectrophotometer with DTGS KBr detector. The number of scans is 32, the resolution is 4 cm-1 and scan rate is 1.928 cm-1 step-1. The samples were mixed with KBr at the ratio of 1:180 and pelletized. The X-ray photoelectron spectra (XPS) were measured with an ANELVA AES-430S X-ray photoelectron spectrometer and the binding energy of C 1s was shifted to 284.6 eV as an internal reference.

SSB preparation The two stabilizers were added to the oven dried and sieved SS at the rates of 1%, 2%, and 4% on a dry weight basis. After thoroughly mixed, the mixtures were carbonized at 350 oC for 1 h. The carbonization temperature of 350 oC was selected because our previous study [1] showed that the stabilizers were most effective in reducing availabilities of the heavy metals at this temperature. The loss of thermal conversion for SS samples are shown in S1 Fig (Supporting Information), and at 350 oC for 1 h, the weight loss is approximately 20%. The obtained biochars were labeled as SSBFA1, SSBFA2, and SSBFA4 for FA incorporation at 1%, 2%, and 4%, respectively and as SSBCS1, SSBCS2, and SSBCS4 for CS incorporation at 1%, 2%, and 4%, respectively.

Heavy metal uptake by plants The soil culture experiment was conducted in the SCAU greenhouse in Guangzhou (113.368926E, 23.16368N) with the natural daylight (the light intensity 20–300 lx during the daytime). The temperatures during the pot study are between 25–36˚C, and moisture was adjusted to 65% of field holding capacity. In pot experiments, a total of 7 treatments were set up in four replicates: CK, SS, SSB, SSBFA2, SSBFA4, SSBCS2, and SSBCS4. For CK, no SS or SSB was applied. For treatment SS, SS but not SSB was applied. For the other five treatments, the corresponding SSB was applied. For each pot, 4 kg air dried soil was used (The size of pot: the upper diameter is 20 cm, the lower diameter is 15 cm, the height is 18 cm, and 18 kg soil/ pot); sewage sludge or biochars were applied at 0.5% on a dry weight basis; basic fertilizers of 1.13 g urea, 0.65 g ammonium dihydrogen phosphate and 0.8 g potassium chloride were applied. Soil, sewage sludge/biochar, and fertilizers were mixed thoroughly before being put into each pot, and moisture was adjusted to 65% of field holding capacity. The design of this study can be intuitively displayed in Fig 1. On August 30th, 2013, 3 seeds of waxy corn (Zea mays L. ceratina Kulesh) were sown in each pot. At the 3rd day after germination, the seedlings were thinned with only 2 seedlings left in each pot. During the whole experiment, the plants were watered once per day with 200 ml water/pot for the first 20 days and twice per day with 300 ml water each time at the later stage.


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Fig 1. Schematic representation of the experiment design. https://doi.org/10.1371/journal.pone.0183617.g001

The aboveground parts of the corn plants were harvested at the 45th day after germination. Both fresh and oven dried weights of the harvested corn plants were recorded. To determine the heavy metal contents of the plants, subsamples of the dried plants were ashed in a muffle furnace at 550 oC for 6 h, and after cooled, the ashed samples were extracted with 1:1 hydrochloric acid solution and filtrated. The filtrates were measured for the concentrations of Zn, Pb, Cd, and Ni using an atomic absorption spectrophotometer (Z-2300, HITACHI).

Chemical analysis and data analysis For total heavy metal concentration determination, the samples of SS, SSB, stabilizers and soil were digested with HF-HNO3-HClO4, and concentrations of Zn, Pb, Cd, and Ni in the digested solution were determined using the AAS. Available heavy metals in the samples were estimated by the DTPA-CaCl2-TEA extraction method [14]. Briefly, metals were extracted with a solution containing 0.005 M DTPA, 0.1 M triethanolamine (TEA) and 0.01 M CaCl2 at the soil: solution ratio of 1:5; pH of the resulting solution was adjusted to 7.30 with diluted HCl solution; concentrations of heavy metals in the extracts were determined using the AAS. The chemical speciation (acid extractable fraction, reducible fraction, oxidizable fraction and residual fraction) for heavy metals from SS and SSBs were measure using the optimized BCR sequential extraction procedure [15]. Data were analyzed by ANOVA and differences between treatments were tested by Duncan’s multi-range test (P = 0.05) using SAS software (version 8.2, SAS Institute, 2004).


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Results and discussion Total heavy metal concentration in SBBs Carbonization raised total heavy metal concentrations in the SS due to loss of volatile components (Table 1 and Fig 2). The contents of Zn and Ni increased by 16.6 and 29.5%, respectively; while those of Pb and Cd increased by 1.6% and 6.3%, respectively after SS carbonization. None of the heavy metal concentrations of the SSB exceeded the critical levels for

Fig 2. Total heavy metal concentrations in raw SSB (0% stabilizer) and SSB with FA or CS incorporated at 1%, 2% or 4%. https://doi.org/10.1371/journal.pone.0183617.g002


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sludge application in agriculture in China (GB4284-84). Similar results were reported by Koppolu et al. [16] that concentrations of Cu, Zn, Ni, Cr, and Co increased by four to six times in biochar relative to its feedstock. Incorporation of stabilizers significantly decreased total heavy metal concentrations in the SSB (P